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Avoiding incidental predation by mammalian herbivores: accurate detection and efficient response in aphids

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Abstract

Mammalian herbivores eat plants that may also provide food and shelter for insects. The direct trophic effect of the browsing and grazing of mammalian herbivory on insects, which is probably prevalent in terrestrial ecosystems, has been mostly neglected by ecologists. We examined how the aphid Uroleucon sonchi L. deals with the danger of incidental predation by mammalian herbivores. We found that most (76%) of the aphids in a colony survive the ingestion of the plant by a feeding herbivore. They do so by sensing the combination of heat and humidity in the herbivore’s breath and immediately dropping off the plant in large numbers. Their ability to sense the herbivore’s breath or their tendency to drop off the plant weakens as ambient temperature rises. This could indicate a limitation of the aphids’ sensory system or an adaptation that enables them to avoid the hostile conditions on a hot ground. Once on the ground, U. sonchi is highly mobile and capable of locating a new host plant by advancing in a pattern that differs significantly from random movement. The accurate and efficient defense mechanism of U. sonchi emphasizes the significance of incidental predation as a danger to plant-dwelling invertebrates.

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References

  • Alyokhin A, Sewell G (2003) On-soil movement and plant colonization by walking wingless morphs of three aphid species (Homoptera: Aphididae) in greenhouse arenas. Environ Entomol 32:1393–1398

    Article  Google Scholar 

  • Beauchamp G (2007) Exploring the role of vision in social foraging: what happens to group size, vigilance, spacing, aggression and habitat use in birds and mammals that forage at night? Biol Rev 82:511–525

    Article  PubMed  Google Scholar 

  • Blackman RL, Eastop VF (2006) Aphids on the world's herbaceous plants and shrubs. John Wiley & Sons, Chichester

    Google Scholar 

  • Bonal R, Muñoz A (2007) Multi-trophic effects of ungulate intraguild predation on acorn weevils. Oecologia 152:533–540

    Article  PubMed  Google Scholar 

  • Carver M (1999) Uroleucon sonchi (Linnaeus) (Hemiptera: Aphididae) in Australia. Aust J Entomol 38:314–317

    Article  Google Scholar 

  • Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu Rev Entomol 47:267–297

    Article  PubMed  CAS  Google Scholar 

  • Conner J, Camazine S, Aneshansley D, Eisner T (1985) Mammalian breath: trigger of defensive chemical response in a tenebrionid beetle (Bolitotherus cornutus). Behav Ecol Sociobiol 16:115–118

    Article  Google Scholar 

  • Cooper WE Jr (2009) Rapid covering by shadow as a cue to predation risk in three lizard species. Behaviour 146:1217–1234

    Article  Google Scholar 

  • Cork A (1996) Olfactory basis of host location by mosquitoes and other haematophagous Diptera. In: Bock GR, Cardew G (eds) Olfaction in mosquito-host interactions, Ciba Foundation Symposium 200. John Wiley & Sons, Chinchester, pp 71–88

    Google Scholar 

  • Dempster JP (1997) The role of larval food resources and adult movement in the population dynamics of the orange-tip butterfly (Anthocharis cardamines). Oecologia 111:549–556

    Article  Google Scholar 

  • Dill LM, Fraser AHG, Roitberg BD (1990) The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia 83:473–478

    Article  Google Scholar 

  • Dixon AFG (1958) The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L.). Trans R Entomol Soc Lond 110:319–334

    Article  Google Scholar 

  • Dixon AFG (1998) Aphid ecology: an optimization approach. Chapman and Hall, London

    Google Scholar 

  • Dixon MD, Johnson WC, Adkisson CS (1997) Effects of weevil larvae on acorn use by blue jays. Oecologia 111:201–208

    Article  Google Scholar 

  • Drew RAI (1987) Reduction in fruit fly (Tephritidae: Dacinae) populations in their endemic rainforest habitat by frugivorous vertebrates. Aust J Zool 35:283–288

    Article  Google Scholar 

  • Eisner T, Grant RP (1981) Toxicity, odor aversion, and "olfactory aposematism". Science 213:476

    Article  PubMed  CAS  Google Scholar 

  • Ferrer LM, Ortín A, Loste A, Fernández A, Verde MT, Ramos JJ (2007) Photosensitisation in sheep grazing alfalfa infested with aphids and ladybirds. Vet Rec 161:312–314

    Article  PubMed  CAS  Google Scholar 

  • Fraenkel GS (1959) The raison d'être of secondary plant substances. Science 129:1466–1470

    Article  PubMed  CAS  Google Scholar 

  • Francke DL, Harmon JP, Harvey CT, Ives AR (2008) Pea aphid dropping behavior diminishes foraging efficiency of a predatory ladybeetle. Entomol Exp Appl 127:118–124

    Article  Google Scholar 

  • Gish M, Inbar M (2006) Host location by apterous aphids after escape dropping from the plant. J Insect Behav 19:143–153

    Article  Google Scholar 

  • Gish M, Dafni A, Inbar M (2010) Mammalian herbivore breath alerts aphids to flee host plant. Curr Biol 20:R628–R629

    Article  PubMed  CAS  Google Scholar 

  • Hartbauer M (2010) Collective defense of Aphis nerii and Uroleucon hypochoeridis (Homoptera, Aphididae) against natural enemies. PLoS One 5:e10417

    Article  PubMed  Google Scholar 

  • Hawkins BA, Cornell HV, Hochberg ME (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–2152

    Article  Google Scholar 

  • Herrera CM (1984) Avian interference of insect frugivory: an exploration into the plant-bird-fruit pest evolutionary triad. Oikos 42:203–210

    Article  Google Scholar 

  • Huffman DW, Laughlin DC, Pearson KM, Pandey S (2009) Effects of vertebrate herbivores and shrub characteristics on arthropod assemblages in a northern Arizona forest ecosystem. Forest Ecol Manag 258:616–625

    Article  Google Scholar 

  • Inbar M, Izhaki I, Koplovich A, Lupo I, Silanikove N, Glasser T, Gerchman Y, Perevolotsky A, Lev-Yadun S (2010) Why do many galls have conspicuous colors? A new hypothesis. Arthropod-Plant Inte 4:1–6

    Article  Google Scholar 

  • Jones AS, Lamont BB, Fairbanks MM, Rafferty CM (2003) Kangaroos avoid eating seedlings with or near others with volatile essential oils. J Chem Ecol 29:2621–2635

    Article  PubMed  CAS  Google Scholar 

  • Kruess A, Tscharntke T (2002) Contrasting responses of plant and insect diversity to variation in grazing intensity. Biol Conserv 106:293–302

    Article  Google Scholar 

  • Launchbaugh KL, Provenza FD, Pfister JA (2001) Herbivore response to anti-quality factors in forages. J Range Manage 54:431–440

    Article  Google Scholar 

  • Lazzari CR (2009) Orientation towards hosts in haematophagous insects: an integrative perspective. Adv Insect Physiol 37:1–58

    Article  Google Scholar 

  • Lehane MJ (2005) The biology of blood-sucking in insects. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Losey JE, Denno RF (1998a) Interspecific variation in the escape responses of aphids: effect on risk of predation from foliar-foraging and ground-foraging predators. Oecologia 115:245–252

    Article  Google Scholar 

  • Losey JE, Denno RF (1998b) The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecol Entomol 23:53–61

    Article  Google Scholar 

  • Malavasi S, Georgalas V, Mainardi D, Torricelli P (2008) Antipredator responses to overhead fright stimuli in hatchery-reared and wild European sea bass (Dicentrarchus labrax L.) juveniles. Aquacult Res 39:276–282

    Article  Google Scholar 

  • Mann JA, Tatchell GM, Dupuch MJ, Harrington R, Clark SJ, McCartney HA (1995) Movement of apterous Sitobion avenae (Homoptera: Aphididae) in response to leaf disturbances caused by wind and rain. Ann Appl Biol 126:417–427

    Article  Google Scholar 

  • Mellanby K (1958) The alarm reaction of mosquito larvae. Entomol Exp Appl 1:153–160

    Article  Google Scholar 

  • Mortola JP, Lanthier C (2005) Breathing frequency in ruminants: a comparative analysis with non-ruminant mammals. Resp Physiol Neurobi 145:265–277

    Article  Google Scholar 

  • Narayandas GK, Alyokhin AV (2006) Interplant movement of potato aphid (Homoptera: Aphididae) in response to environmental stimuli. Environ Entomol 35:733–739

    Article  Google Scholar 

  • Nunamaker RA, Lockwood JA, Stith CE, Campbell CL, Schell SP, Drolet BS, Wilson WC, White DM, Letchworth GJ (2003) Grasshoppers (Orthoptera: Acrididae) could serve as reservoirs and vectors of vesicular stomatitis virus. J Med Entomol 40:957–963

    Article  PubMed  Google Scholar 

  • Odeyinka SM (2000) Feeding behaviour and diet selection by West African Dwarf Goats. Arch Tierz 43:57–61

    Google Scholar 

  • Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81–105

    Article  Google Scholar 

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330

    Article  Google Scholar 

  • Provenza FD (1995) Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J Range Manage 48:2–17

    Article  Google Scholar 

  • Rambo JL, Faeth SH (1999) Effect of vertebrate grazing on plant and insect community structure. Conserv Biol 13:1047–1054

    Article  Google Scholar 

  • Redford KH, Bouchardet da Fonseca GA, Lacher TE (1984) The relationship between frugivory and insectivory in primates. Primates 25:433–440

    Article  Google Scholar 

  • Roitberg BD, Myers JH (1979) Behavioural and physiological adaptations of pea aphids (Homoptera: Aphididae) to high ground temperatures and predator disturbance. Can Entomol 111:515–519

    Article  Google Scholar 

  • Roitberg BD, Myers JH, Frazer BD (1979) The influence of predators on the movement of apterous pea aphids between plants. J Anim Ecol 48:111–122

    Article  Google Scholar 

  • Rooney TP, Waller DM (2003) Direct and indirect effects of white-tailed deer in forest ecosystems. Forest Ecol Manag 181:165–176

    Article  Google Scholar 

  • Ruth WE, McNew RW, Caves DW, Eikenbary RD (1975) Greenbugs [Hom.: Aphididae] forced from host plants by Lysiphlebus testaceipes [Hym.; Braconidae]. Entomophaga 20:65–71

    Article  Google Scholar 

  • Sallabanks R, Courtney SP (1992) Frugivory, seed predation, and insect-vertebrate interactions. Annu Rev Entomol 37:377–400

    Article  PubMed  CAS  Google Scholar 

  • Spinhirne JP, Koziel JA, Chirase NK (2004) Sampling and analysis of volatile organic compounds in bovine breath by solid-phase microextraction and gas chromatography-mass spectrometry. J Chromatogr A 1025:63–69

    Article  PubMed  CAS  Google Scholar 

  • Stewart AJA (2001) The impact of deer on lowland woodland invertebrates: a review of the evidence and priorities for future research. Forestry 74:259–270

    Article  Google Scholar 

  • Suominen O, Danell K, Bryant JP (1999) Indirect effects of mammalian browsers on vegetation and ground-dwelling insects in an Alaskan floodplain. Ecoscience 6:505–510

    Google Scholar 

  • Takken W, Knols BGJ (1999) Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44:131–157

    Article  PubMed  CAS  Google Scholar 

  • Taweel HZ, Tas BM, Smit HJ, Tamminga S, Elgersma A (2006) A note on eating behaviour of dairy cows at different stocking systems—diurnal rhythm and effects of ambient temperature. Appl Anim Behav Sci 98:315–322

    Article  Google Scholar 

  • Traveset A, Willson MF, Gaither JC Jr (1995) Avoidance by birds of insect-infested fruits of Vaccinium ovalifolium. Oikos 73:381–386

    Article  Google Scholar 

  • Tscharntke T (1997) Vertebrate effects on plant-invertebrate food webs. In: Gange AC, Brown VK (eds) Multitrophic interactions in terrestrial systems. Blackwell Science Ltd., Oxford, pp 277–297

    Google Scholar 

  • Valburg LK (1992) Eating infested fruits: interactions in a plant–disperser–pest triad. Oikos 65:25–28

    Article  Google Scholar 

  • Vourc'h G, De Garine-Wichatitsky M, Labbé A, Rosolowski D, Martin J-L, Fritz H (2002) Monoterpene effect on feeding choice by deer. J Chem Ecol 28:2411–2427

    Article  PubMed  Google Scholar 

  • Wallach AD, Shanas U, Inbar M (2010) Feeding activity and dietary composition of roe deer at the southern edge of their range. Eur J Wildl Res 56:1–9

    Article  Google Scholar 

  • Yamazaki K, Sugiura S (2008) Deer predation on leaf miners via leaf abscission. Naturwissenschaften 95:263–268

    Article  PubMed  CAS  Google Scholar 

  • Zamora R, Gómez JM (1993) Vertebrate herbivores as predators of insect herbivores: an asymmetrical interaction mediated by size differences. Oikos 66:223–228

    Article  Google Scholar 

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Acknowledgments

We would like to thank Toby Gish and Marcia Ford for the editorial assistance and Prof. Ido Izhaki for the statistical advice.

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Correspondence to Moshe Inbar.

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Communicated by: Sven Thatje

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Gish, M., Dafni, A. & Inbar, M. Avoiding incidental predation by mammalian herbivores: accurate detection and efficient response in aphids. Naturwissenschaften 98, 731 (2011). https://doi.org/10.1007/s00114-011-0819-7

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  • DOI: https://doi.org/10.1007/s00114-011-0819-7

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